Letter

Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen

  • Nature Plants volume 2, Article number: 16153 (2016)
  • doi:10.1038/nplants.2016.153
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Abstract

Plant pathogenic fungi represent the largest group of disease-causing agents on crop plants, and are a constant and major threat to agriculture worldwide. Recent studies have shown that engineered production of RNA interference (RNAi)-inducing dsRNA in host plants can trigger specific fungal gene silencing and confer resistance to fungal pathogens1,​2,​3,​4,​5,​6,​7. Although these findings illustrate efficient uptake of host RNAi triggers by pathogenic fungi, it is unknown whether or not such an uptake mechanism has been evolved for a natural biological function in fungus–host interactions. Here, we show that in response to infection with Verticillium dahliae (a vascular fungal pathogen responsible for devastating wilt diseases in many crops) cotton plants increase production of microRNA 166 (miR166) and miR159 and export both to the fungal hyphae for specific silencing. We found that two V. dahliae genes encoding a Ca2+-dependent cysteine protease (Clp-1) and an isotrichodermin C-15 hydroxylase (HiC-15), and targeted by miR166 and miR159, respectively, are both essential for fungal virulence. Notably, V. dahliae strains expressing either Clp-1 or HiC-15 rendered resistant to the respective miRNA exhibited drastically enhanced virulence in cotton plants. Together, our findings identify a novel defence strategy of host plants by exporting specific miRNAs to induce cross-kingdom gene silencing in pathogenic fungi and confer disease resistance.

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Acknowledgements

We thank B. Scott for plasmid pPN94, Y.-L. Peng for plasmids pKOV21, G.-L. Tang for STTM166 Arabidopsis seeds, and B. Thomma for the VdLs17 strain. This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11040500) and the China Transgenic Research and Commercialization Key Special Project (2014ZX00800908B).

Author information

Author notes

    • Tao Zhang
    • , Yun-Long Zhao
    •  & Jian-Hua Zhao

    These authors contributed equally to this work.

Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

    • Tao Zhang
    • , Yun-Long Zhao
    • , Jian-Hua Zhao
    • , Sheng Wang
    • , Yun Jin
    • , Zhong-Qi Chen
    • , Yuan-Yuan Fang
    • , Chen-Lei Hua
    •  & Hui-Shan Guo
  2. College of Life Sciences, University of the Chinese Academy of Sciences, Beijing 100049, China

    • Tao Zhang
    • , Yun-Long Zhao
    •  & Hui-Shan Guo
  3. Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California, Riverside, California, 92521, USA

    • Shou-Wei Ding

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Contributions

H.S.G. and T.Z. designed experiments. T.Z., Y.L.Z. and S.W. performed experiments. J.H.Z. performed sRNA computational informatics analysis. J.Y. assisted with the 5′-RACE assay. Y.Y.F. and Z.Q.C provided technical support. H.S.G., J.H.Z., T.Z. and Y.L.Z. analysed data. H.S.G., S.W.D., C.L.H. and T.Z. discussed the results and wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Hui-Shan Guo.

Supplementary information

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    Supplementary Information

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